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If a male songbird is worried about his mate's fidelity, should he react violently towards a rival male, or should he sing a duet with his mate when a rival shows up? A newly published study of the red-backed fairy-wren, a highly promiscuous species with high rates of extra-pair paternity, reveals that physical aggression towards an intruder accomplished nothing, whereas males who sang a duet with their mate had a significantly higher rate of paternity. These results suggest that song duets acted either as acoustic mate-guarding or as male–female vocal negotiations that lead to increased paternity.

The red-backed fairy-wren, Malurus melanocephalus, is a small effervescent songbird that lives in the semi-arid savannahs and scrublands of northern and northeastern Australia. They primarily consume insects, although they will eat small fruits and seeds when they can find them. These birds are strongly territorial: both sexes will team up in a coordinated display to vigorously defend their territory from intruders.

The red-backed fairy-wren shows strong sexual dichromatism, where males and females have strikingly different plumage colours and patterns. Adult males are coal-black with a red or orange patch on their backs whereas females and juveniles have tan upperparts and cream-coloured underparts.

Breeding season extends from August to February -- coinciding with the rainy season in northern Australia when limited food resources reach their peak. Red-backed fairy-wrens live in groups where some of the young from a previous nest will stick around to help their parents raise the next group of chicks. Although this species is socially monogamous, both males and females are highly promiscuous, and males who have fathered chicks outside of the pair bond often help raise their "extra-pair" youngsters -- a situation that encourages all sorts of intricate social relationships. Thus, these birds provide scientists with a fascinating social system for learning about the process of speciation and the evolution of mate selection in birds.

"I was interested in sexual selection and speciation in birds and became interested in fairy-wrens when I first met my eventual PhD advisor Mike Webster", said the lead author of the study, evolutionary biologist Daniel Baldassarre, an NSF Postdoctoral Research Fellow at the University of Miami's Department of Biology. Dr Baldassarre was a grad student at Cornell University when this study was conducted.

"I thought that they sounded like a really good excuse to go traipse around the Australian outback", said Dr Baldassarre in email.

Molecular biology has deepened our knowledge of nature and of evolution in many surprising ways. For example, thanks to DNA fingerprinting and other molecular techniques, we now know that most bird species that form a monogamous pair-bond are really only socially monogamous; they very rarely are sexually monogamous (doi:10.1046/j.1365-294X.2002.01613.x), as was long thought. So how can a male bird protect his paternity in the offspring that he cares for? Careful observation reveals that male songbirds rely upon aggressive displays -- either physical aggression or vocal displays (or both) -- to protect their paternity. But do such displays actually work, especially in such an enthusiastically promiscuous species like the red-backed fairy-wren? Is physical aggression more effective than a vocal display, such as singing a duet with one's mate?

To answer these questions, Dr Baldassarre and his team designed a study to test whether paternity could be tied more closely to physical aggression or to vocal displays (duetting in this case) in wild red-backed fairy-wrens. As part of this work, the team created a variety of mounts, or fake fairy-wrens, from a combination of clay, synthetic feathers and real back and tail feathers contributed by previously captured fairy-wrens.

"When we first put out the mounts in the field, we were worried that the birds would not be fooled, and would realize they were not real birds and thus not respond properly. But on one of the first mornings of our pilot experiments, a pied butcherbird, one of the main predatory birds that attacks fairy-wren[s], came out of nowhere, attacked the mount, ripped the tail off, and tried to carry it away", said Dr Baldassarre.

"Although our mount was destroyed, we were thrilled because it was good evidence that the mounts were being perceived as real birds."

So a hungry predator was fooled, but how did the fairy-wrens react?

"Then we discovered that the fairy-wrens themselves would respond quite aggressively to the mounts", said Dr Baldassarre. "The key seemed to be the addition of feathers, which gave the mounts a lifelike texture." He went on to note that the study birds did not respond to featherless mounts with the same size, shape, and colours.

In this video, you can hear the resident male red-backed fairy-wren singing loudly before launching a vigorous (vicious?) attack upon a decoy that was attached to a branch within his territory. Most interesting (to me, at least), is the subsequent clip of a resident male who also attacked the blue-and-white decoy, which looks nothing like a rival red-backed fairy-wren:

"One male was so aggressive, he would violently attack every mount for upwards of 15 minutes", added Dr Baldassarre. "We nicknamed him 'face-ripper'."

But despite Face-ripper's exceptional passion for extreme violence, most of the resident males' physical aggression was brief. Instead, the resident pair responded aggressively by singing a duet:

The couple that sings together has more of their own chicks in their nest

Dr Baldassarre and his team conducted paternity tests on the chicks in each pair's nest by analysing seven different DNA segments comprised of repeated sequences of nucleotides, known as microsatellites. Using this method, they were able to identify the genetic paternity for 97% (181/186) of all their study birds' chicks. Of these, the researchers found that 47% of offspring (88/186) were extra-pair young (EPY), and 60% (44/73) of the study nests contained at least one EPY.

Dr Baldassarre and his team compared the resident male's physical aggression levels, the frequency of the resident pair's duetting behaviour with the rate of cuckoldry. They found that resident pairs that spent most of their time singing a duet in response to a decoy rival (Figure 1a) had more of their own genetic offspring in their nests than did those pairs where the resident male spent most of his time being physically aggressive (Figure 1b):

Figure 1. Relationships between duetting (a), aggression (b) and proportion of EPY in a male’s nest. X-values were scaled 0–1 for visualization only, scaling did not transform the data. (Online version in colour.) (Credit: Baldassarre et al. doi:10.1098/rsbl.2015.1025)

"The most surprising result was that physical aggression was not related to cuckoldry at all", said Dr Baldassarre.

"We definitely thought that the hyper-aggressive males, like face-ripper, would be more successful than timid males at maintaining their own paternity", said Dr Baldassarre. "But aggression was not related to paternity, rather, duetting seemed to be the key."

In most bird species where the male and female sing duets, this behaviour is used to strengthen the pair bond -- or perhaps the male is simply "out shouting" the singing female to prevent her from finding an extra-pair copulation. So which scenario might be the situation for red-backed fairy-wrens?

"We think it is one of those two scenarios, but we can’t yet say for sure", said Dr Baldassarre. "Our research group is planning another study to try and figure this out. The key will be discovering who is initiating the duet and who is following. For example, if the female typically starts the duet and then the male immediately joins in, the 'out shouting' behavior (acoustic mate guarding is the jargon) is most likely."

Because song serves many purposes in songbirds, it's difficult to say for sure why duetting evolved in songbirds in the first place.

"Either way, duetting very likely evolved to mediate mating decisions in some way, although it also serves other functions, such as territory defense."

But nevertheless, this is the first study to show a direct relationship between increased duetting behaviour and increased genetic paternity.

"This pattern has been hypothesized many times, and there is some indirect evidence from other studies showing things like the seasonal duet rate increas[es] during the female’s fertile period, but this is the most direct evidence", said Dr Baldassarre.

"In the fairy-wrens, there is very strong selection on males to evolve behaviors to increase their paternity assurance, and duetting seems to be the main way they can do this."